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Effects of Carboxylesterase Gene Silence on Wheat Aphid Sitobion Avenae (Fabricius)

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Effects of Carboxylesterase Gene Silence on Wheat Aphid Sitobion Avenae (Fabricius) Journal of Asia-Pacific Entomology 19 (2016) 341–345 Contents lists available at ScienceDirect Journal of Asia-Pacific Entomology journal homepage: www.elsevier.com/locate/jape Effects of carboxylesterase gene silence on wheat aphid Sitobion avenae (Fabricius) Yifan Zhang a,1, Fei Deng a,1, Yongliang Fan b, Zhangwu Zhao a,⁎ a Department of Entomology, China Agricultural University, Beijing 100193, China b State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi 712100, China article info abstract Article history: Multifunctional carboxylesterase (CarE) has been found in all animals, plants and microbes, and belongs to a Received 5 November 2015 superfamily enzyme of serine hydrolase involved in detoxification, allelochemical tolerance and some specific Revised 21 February 2016 hormone or pheromone metabolism. Insects usually utilize carboxylesterases to detoxify xenobiotics, and posi- Accepted 23 March 2016 tively correlated with insect resistance to some insecticides. Despite the importance of CarEs in insects, Available online 31 March 2016 carboxylesterases and their functions in wheat aphid Sitobion avenae (Fabricius) have not been clear. In this Keywords: study, a sequence that encodes a carboxylesterase protein from S. avenae (SaCarE) was sequenced and cloned. Carboxylesterase After aligning the encoded amino acid sequence of the SaCarE gene with other known CarEs of insects, we RNAi found that the CarE gene was highly conserved in insects. The SaCarE mRNA levels at different developmental Sitobion avenae stages of S. avenae were gradually increased from the first instar of nymphs to adult stage. RNAi was employed Wheat aphid to further explore its functions, in which oral ingestion of SaCarE double-stranded RNA from the third instar nymph significantly knocked down SaCarE expression, and significantly decreased ecdysis index in S. avenae. These results indicate that SaCarE is functional in S. avenae and could serve one of the potential target genes for management of S. avenae. © 2016 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved. Introduction carboxylesterase in antennae of Spodoptera littoralis could metabolize smell matters of plant leaf (Durand et al., 2010). Other studies found Carboxylesterase (CarE) widely exists in animals, plants and micro- that antennae rich in esterase are associated with the degradation of organisms (Satoh and Hosokawa, 1998; Marshall et al., 2003; Miyazaki the ester type of sex pheromone in Apis mellifera (Kamikouchi et al., et al., 2003; Furihata et al., 2004). It is one group of important enzymes 2004) and in two pest moths, Spodoptera littoralis and Sesamia involved in insect detoxification, and plays an important role in insect nonagrioides (Maïbèche-Coisne et al., 2004). Reports indicate that resistance mechanism. When insects are exposed to exogenous harmful carboxylesterase plays an important role in the formation and develop- materials such as medicine, pesticide, herbicide, phenols, alkaloids and ment of the neural regulation, in which carboxylesterase participated in plant secondary metabolites, the activity of carboxylesterase increases neural development adjustment in bees (Biswas et al., 2010). The ac- and the adaptability of insects is enhanced. Studies have found tions of CarE to exogenous and endogenous compounds are through that many insects resistance to organophosphorus insecticide agents degrading sulphur ester keys, amide keys and ester bond hydrolyze were associated with excessive expression of a carboxylesterase gene (Miyazaki et al., 2003). (Vaughan and Hemingway, 1995; Karunaratne et al., 1999). CarE Distribution of carboxylesterase in insects is different. The larval activity reflects the resistance of the peach aphid Myzus persicae to carboxylesterase are mainly distributed in intestine, fat body, body organophosphate, carbamate and pyrethroid pesticides (Bizzaro et al., wall, malpighian tube and other organs, while carboxylesterase of 2005). In addition, carboxylesterase is also involved in the degrada- adult worms are mainly distributed in the legs, body wall and tion of insect pheromones and hormones. Durand found that the head. The expression level of CarE also varies in different insects as well as in different developmental stages of insects. Nowadays, carboxylesterase genes in many insects have been cloned, such as ⁎ Corresponding author at: Department of Entomology, College of Agriculture and M. persicae, Aphis gossypii, Rhopalosiphum padi, Spodoptera frugiperda, Biotechnology, China Agricultural University, Beijing 100193, China. Tel./fax: +86 10 Spodoptera exigua, Helicoverpa armigera (Blackman et al., 1996; Cao 62734225. E-mail address: [email protected] (Z. Zhao). et al., 2008). However, it has not been reported in wheat aphid Sitobion 1 These authors contributed equally to this work. avenae (Fabricius), and its function is still unclear. In order to http://dx.doi.org/10.1016/j.aspen.2016.03.011 1226-8615/© 2016 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved. 342 Y. Zhang et al. / Journal of Asia-Pacific Entomology 19 (2016) 341–345 investigate the function of carboxylesterase in S. avenae, we used the DNA Purification Kit (Tiangen, Beijing, China). The dsRNA was synthe- RNAi to knock down the gene expression and observed its effects on sized by following the instructions of T7 RiboMAX™ Express RNAi Sys- growth and development of the wheat aphid. tem Kit, and was further purified and quantified by spectrophotometer at 260 nm. Materials and methods CarE expression analysis at different instars of nymphs and adults Insects To study temporal expression of CarE during the different develop- The colony of wheat aphid, S. avenae (Fabricius), was a laboratory mental stages, we explored different instars of larvae and adults. The strain kindly provided by Dr. Dunlun Song, China Agricultural University. temporal expression of CarE in S. avenae was estimated by qRT-PCR Aphids were reared on wheat seedlings at 22 ± 1 °C under a 16:8 h using RealMasterMix (SYBR Green) on StepOne™ Real-time PCR System light/dark photoperiod with new wheat seedlings provided once a week. (USA). The primers for qRT-PCR were designed and shown in Table 1. The ribosomal protein L7 (RpL7) gene showed a stable expression in dif- Cloning of CarE ferent developmental stages (Wang et al., 2012) and was chosen as the control. Cycling for each reaction was carried out in a final volume of Total RNA was extracted from the whole body of adult aphids using 20 μl containing 1 μl of the cDNA sample, 0.6 μl (10 pmol/μl) of each the TRIzol Reagent (Tiangen, Beijing, China). Extracted RNA concentra- primer, 10 μl 2× SuperReal PreMix Plus, 2 μl 50× ROX Reference Dye tion and purity was determined by spectrophotometry-NanoDrop 2000 and 5.8 μlddH2O. (Thermo Scientific, Pittsburgh, PA). The synthesis of cDNA was per- The amplification efficiency of the gene was estimated by primer ef- formed with Fast Quant RT Kit (Tiangen, Beijing, China) according to ficiency test. The PCR program consisted of an initial denaturation at the manufacturer's instructions. CarE coding sequence was amplified 95 °C for 15 min followed by 40 cycles of denaturation at 94 °C for from S. avenae cDNA by PCR using 2×Taq PCR MasterMix Kit (Aidlab 10 s, annealing at 57 °C for 20 s and elongation at 72 °C for 30 s. An Biotechnologies, Beijing, China) with degenerate primers (Table 1). actin fragment was amplified as an internal control. Relative expression The PCR was performed at 94 °C for 3 min, followed by 35 cycles of of the CarE gene in different stages was conducted according to thresh- 94 °C for 30 s, 55 °C for 30 s and 72 °C for 30 s, finished with an extension old cycle (Ct) value based on the 2−△△CT method. Each experiment was step at 72 °C for 10 min. PCR products were run on 1.5% agarose gel and independently repeated three times and three technical replicates were stained with ethidium bromide. PCR products were purified using performed in each of these three biological repetitions. All values were Universal DNA Purification Kit (Tiangen, Beijing, China). The purified the means of three individual measurements ±SE. All the data are fragments were cloned into PMD19-T Simple vector and transformed presented as the relative mRNA expression. into Escherichia coli DH5α cells. Feeding effects of dsCarE Sequence analysis The diet used for rearing S. avenae was a meridic artificial diet The CarE sequences of S. avenae were blasted at NCBI website (see Deng and Zhao, 2014). The nymphs of the third instar were fed (http://www.ncbi.nlm.nih.gov/) to ensure that no more than a 20-bp on three different dsCarE-containing diets (5, 10 and 20 ng/μl), and homology existed between the CarE sequences and any other genes in mortality was respectively recorded every day. A total of 15 individuals S. avenae. The CarE sequence was translated into protein with online were transferred into a vial using a soft writing brush and the vial was software (http://insilico.ehu.es/translate/) to establish the degree of sealed with stretched Parafilm. The diet containing dsCarE (2 μl dsCarE similarity and conservation among different CarE orthologs. were added to every 100 μl artificial diets, which were changed every two days) was fed to the nymphs until the fourth day for expression Preparation of dsRNA analysis of CarE. From the background experiments above, 20 ng/μl concentration of dsCarE was selected to investigate the effects on the The dsRNAs were synthesized in vitro with T7 RiboMAX™ Express aphids, and dsGFP of the same concentration was also mixed into RNAi System (Promega, USA). A CarE coding fragment of 312 bp was artificial diet to serve as control. The isometric DEPC H2O was mixed selected as RNAi target sequence. PCR primers with T7 promoter into artificial diet to serve as another control.
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